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Intraspecific Shore-Level Size Gradients in Intertidal MolluscsAuthor(s): Geerat J. VermeijReviewed work(s):Source: Ecology, Vol. 53, No. 4 (Jul., 1972), pp. 693-700Published by: Ecological Society of AmericaStable URL: http://www.jstor.org/stable/1934785 .Accessed: 26/10/2012 11:03

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INTRASPECIFIC SHORE-LEVEL SIZE GRADIENTS IN INTERTIDAL MOLLUSCS'

GEERAT J. VERMEIJ

Department of Zoology, University of Maryland, College Park, Maryland 20742

Abstract. A synthesis of new data and literature observations indicates that, within rocky intertidal gastropod species (1) shell size tends to increase in an upshore direction in species characteristic of the littoral fringe and in high intertidal limpets, and (2) shell size often decreases in an upshore direction in species typical of lower intertidal levels. These size gradients are considered to be a response to gradients in the intensity and nature of postlarval prereproductive mortality on the shore. In gastropods whose size gradients are of type 1, mortality generally resulting from physical extremes operates from above and is most effective against small individuals. Among snails with size gradients of type 2, mortality often in the form of predation or other biotic interaction is most intense at low levels. Sedentary species can become graded according to size with shore level only through differential mortality of one size group relative to another over the entire vertical range of the species, while mobile forms may become size segregated by active migration of one size group relative to another.

INTRODUCTION

The physical partitioning of different growth stages in different parts of the niche is typical of many animal species and, like morphological lines, can often be correlated with and considered to be a response to environmental gradients in space or time. In the marine intertidal zone, the separation of postlarval life stages is often in the form of a gradient in body size along a vertical transect of the shore. Although many such gradients have been described, very few are adequately understood; and little attempt has been made to correlate the nature and direction of the size gradients with mode of life and habitat.

In conjunction with a study of morphological patterns among high intertidal rocky-shore gastropods (Vermeij, in preparation), samples of species were collected from different shore levels in several localities and were examined for possible shore-level size gradients. In this paper, a summary of these gradients together with those recorded in previous literature is presented, and an interpretation of patterns relating nature and direction of the gradients with mode of life and habitat of the species is suggested.

OBSERVATIONS AND RESULTS

Tables 1 and 2 summarize known size gradients from personal observations and from previous literature in rocky-shore gastropods, based on maximum linear shell dimension. Only those size gradients are considered where juvenile specimens were included in the populations sampled. Size gradients reported for the first time in this paper were observed at all localities in the geographic area indicated where the species in question was found.

Not all gastropods exhibit shore-level size gradients, and many size gradients are likely to have been

1Received December 23, 1971; accepted February 8, 1972.

overlooked. Segal (1956) states that there are no significant size differences between low-level and high- level populations of the limpet Acmaea limatula in southern California, and Abe (1942) failed to find a size gradient in populations of the mangrove snail Littorina scabra in Palau. Size gradients also appear to be lacking in many forms of L. saxatilis in Britain (James 1968).

Some caution is to be exercised in the interpretation of the present data. Allometric changes during ontogeny may slightly alter the correspondence between maximum linear shell dimension and volume or weight. In most limpets there is an increase in cone height relative to major basal diameter (the maximum linear dimension) during growth; hence size data based on the major diameter will tend to under- estimate differences in volume or weight between two samples. On the other hand, data based on the maximum linear dimension of littorinids (distance from apex of shell to farthest point on outer lip) will tend to overestimate weight or volume differences because of allometric increase of spire height relative to aperture length and shell width during ontogeny. I feel, however, that maximum dimension is an adequate, if somewhat crude, measure to determine the presence and nature of size segregation. Shotwell's (1950) data on size gradients in two Californian limpets of the genus Acmaea (see Table 2) are based on volume.

A second, perhaps more serious, difficulty may arise because of differences in growth rate between low-level and high-level individuals of the same species. Newcombe (1935), Seed (1968), and others have shown that growth rate in the mussel Mytilus edulis is much lower at high shore levels than in lower shore habitats; yet high-level individuals, de- spite their small size, are often the oldest members of the population. In the sand-dwelling bivalve Tel-

694 GEERAT J. VERMEIJ Ecology, Vol. 53, No. 4

TABLE 1. Gastropods increasing in size in an upshore direction

Species Vertical range Area References

Acmaeidae Acmaea digitalis high intertidal Oregon, California Frank 1965, Haven 1971 A. scabra high intertidal California Sutherland 1970, Haven 1971 Notaocema mayi high intertidal Tasmania Bennett and Pope 1960

Patellidae Patella vulgata low to high intertidal Great Britain Orton, 1928 Lewis 1954, Blackmore

1969 Fissurellidae

Fissurella barbadensis low to high intertidal Barbados Ward 1967 Trochidae

Gibbula umbilicalis mid to high intertidal Wales, Brittany Bakker 1959, Williams 1964b Neritidae

Nerita quadricolor high intertidal Aldabra Atoll Hughes 1971 N. ascensionis deturpensis mid intertidal to lit- Ilha Fernando de No- Vermeij 1970

toral fringe ronha, Brazil Littorinidae

Littorina angulifera high intertidal, lit- Florida, West Indies Lenderking 1954, GJV toral fringe

L. neritoides high intertidal, lit- Mediterranean Palant and Fishelson 1968, Star- toral fringe mtihlner 1969

L. punctata high intertidal, lit- Mediterranean, Ghana Evans 1961, Palant and Fishelson toral fringe 1968, GJV

L. ziczac brasiliensis high intertidal, lit- Brazil Vermeij and Porter 1971 toral fringe

L. peruviana high intertidal, lit- Peru Vegas 1963 toral fringe

L. africana high intertidal, lit- South Africa Eyre and Stephenson 1938 toral fringe

L. saxatilis rudis high intertidal Great Britain James 1968 L. unifasciata unifasciata high intertidal, lit- New South Wales, Vic- Dakin, Bennett, and Pope 1948,

toral fringe toria, Tasmania Bennett and Pope 1953, 1960 L. u. antipodum high intertidal, lit- New Zealand Morton and Miller 1968

toral fringe L. praetermissa high intertidal, lit- Victoria, Tasmania Bennett and Pope 1953, 1960

toral fringe L. coccinea littoral fringe Society Islands Fischer 1952 L. planaxis high intertidal, lit- California North 1954

toral fringe L. littoreaa low to high intertidal Great Britain Smith and Newell 1955, Williams

1964a Nodilittorina helenae ssp. high intertidal, lit- Ilha Fernando de No- GJV

toral fringe ronha, Brazil N. tuberculata high intertidal, lit- West Indies Lewis 1960, GJV

toral fringe N. miliaris high intertidal, lit- Sierre Leone, Ghana GJV

toral fringe N. millegranaa low intertidal to Ceylon Atapattu 1968

littoral fringe Tectarius muricatus littoral fringe West Indies de Jong and Kristensen 1965

Muricidae Thais distinguenda low to mid intertidal Queensland Endean, Kenny, and Stephensen 1956 Dicathais aegrota subtidal to mid West Australia Phillips 1969

intertidal Siphonariidae

Siphonaria gigass mid to high intertidal west coast Panama GJV S. lessoni high intertidal, lit- Argentina Olivier and Penchaszadeh 1968

toral fringe S. picta mid to high intertidal southern Brazil Marcus and Marcus 1960

aComplex gradient; see text under Obervations.

lina tennis, growth rate is inversely related to population density (Stephen 1928, Trevallion, Edwards, and Steele 1970); since density decreases from low to high shore levels, there is an apparent increase in body size in an upshore direction but no corresponding increase in average age (Stephen 1928). Suther- land (1970) has similarly found an inverse relationship between growth rate and population density in

the limpet Acmaea scabra, but in this case an upshore decrease in density and corresponding increase in growth rate merely reinforce an upshore increase in mean age (Sutherland 1970, Haven 1971). The growth rate of high-level A. scabra was found to be slower than that of low-level individuals when kept at the same population density (Sutherland 1970). Judging from the number of growth rings on the

Summer 1972 SHORE-LEVEL SIZE GRADIENTS 695

TABLE 2. Gastropods decreasing in size in an upshore direction

Species Vertical range Area References

Acmaeidae Acmaea peltaa low to mid intertidal Oregon Shotwell 1950 A. testudinalis testudinalis low to mid intertidal Nova Scotia Stephenson and Stephenson 1954 A. s. scutuma low to mid intertidal Oregon Shotwell 1950 A. noronhensis low to high intertidal Ilha Fernando de No- GJV

ronha, Brazil Patellidae

Patella argenvillei low intertidal west South Africa Stephenson, Stephenson, and Day 1940

P. intermedia mid intertidal Senegal GJV Trochidae

Cittarium pica subtidal to mid West Indies Lewis 1960, GJV intertidal

Tegula funebralis low to mid intertidal Washington Paine 1969, 1971 T. atra low to mid intertidal central Chile GJV Monodonta lineata low to high intertidal Great Britain Desai 1966 Trochus niloticus subtidal to low Guam GJV

intertidal Neritidae

Nerita undata mid to high intertidal Singapore GJV N. scabricosta high intertidal to lit- west coast Panama Vermeij, in prep.

toral fringe N. sanguinolenta low to mid intertidal Red Sea Safriel 1969

Littorinidae Littorina scutulata high intertidal California Bock and Johnson 1967 L. Iittorea low intertidal to Connecticut GJV

littoral fringe L. littoreab low to high intertidal Great Britain Smith and Newell 1955, Williams

1964a Planaxidae

Planaxis planicostatus mid to high intertidal west coast of Panama GJV Muricidae

Morula granulate low to mid intertidal Hawaii GJV Drupa ricina subtidal to mid Hawaii GJV

intertidal Thais haemastoma subtidal to high Senegal GJV

intertidal Ocenebra crassilabrum low to mid intertidal central Chile GJV

aJuveniles throughout vertical range; adults restricted to lower part of range. bComplex gradient; see text under Observations.

shell, size is positively correlated with age in all species in Tables 1 and 2.

Inspection of Tables 1 and 2 reveals two patterns among mobile rocky-shore gastropods: (1) shell size tends to increase in an upshore direction in species characteristic of the littoral fringe and in high intertidal limpets-that is, the largest and oldest individuals are found near the upper limit of vertical distribution of the species; and (2) shell size often tends to decrease in an upshore direction in species typical of lower intertidal levels.

Among Littorinidae, a large number of supratidal species fall into pattern (1), while the high intertidal Littorina scutulata (see Bock and Johnson 1967) exemplifies pattern (2). Littorina littorea in Con- necticut, ranging from below low water to the lower- most littoral fringe, exhibits decreasing mean shell size toward high shore levels (Vermeij, unpublished). The same species on the coast of Kent in Britain exhibits a complex gradient with juveniles apparently living subtidally and adults inhabiting low and mid intertidal levels below second-year individuals (Smith

and Newell 1955). Still another pattern is shown by L. littorea in Wales (Williams 1964a), where juveniles congregate near M. L. W. N., larger and older individuals occurring both above and below this level. This pattern is similar to that described by Atapattu (1968) for "Nodilittorina granularis" (= N. mille- grana), a species ranging throughout the intertidal to the lower littoral fringe on the west coast of Ceylon.

The only apparent exception to the rule that intertidal littorinids should conform to pattern (2) was observed by Bakker (1959), who found that the European intertidal L. obtusata increased in size in an upshore direction. Sacchi (1969a), however, could not detect any size gradient in this species, and points out that Bakker's material actually consisted of two species, the smaller low intertidal L. mariae and the larger mid intertidal L. obtusata.

In limpets (Acmaeidae, Patellidae, Siphonariidae), an intraspecific size decrease toward high shore levels is limited to low and mid intertidal species, while high intertidal species tend to exhibit the opposite size gradient. Most trochids in which size segregation


has been described exhibit an intraspecific size decrease in an upshore direction.

DISCUSSION

The transitional nature of the intertidal habitat from fully marine to fully terrestrial conditions is reflected in the increase in rigor of the physical environment (desiccation, extremes in temperature and salinity) from low to high shore levels. Not only does this gradient result in a pattern of distinct zones of plants and animals at different shore levels, but it may also lead to differences in the degree of interspecific competition, food availability, and predation in different parts of an animal's vertical range (Con- nell 1961a, b, 1970, Paine 1969). We may therefore expect causes of mortality to be different and to act with varying intensities in different parts of the vertical range of a given species.

Suppose now that the intraspecific shore-level size gradients are a response to shore-level gradients in the nature and intensity of mortality. If the mortality gradients have any predictable component, any response to them might be expected to have adaptive significance. Postlarval prereproductives might, because their survival is necessary to the maintenance of the population as a whole, he expected to inhabit the zone of minimal mortality within the vertical range of the species, or else to have a very high growth rate and early maturation if mortality is high or unpredictably variable throughout the species' vertical range. Given the size patterns in the preceding section, and the above assumptions, we might expect the zone of minimal mortality and therefore the greatest concentration of postlarval prereproductives to be at the base of the vertical range of mobile gastropods of the littoral fringe and of high intertidal limpets, and to lie near the top of the vertical range of many lower intertidal gastropods.

Little information is yet available concerning the relative importance and intensity of the various causes of mortality in the intertidal zone. Death resulting from extreme physical conditions near the upper limit of the vertical range is known to occur in many intertidal animals, including barnacles (Con- nell 1961a, b, 1970, Foster 1971), echinoids (Glynn 1968), limpets (Borland 1950, Lewis 1954, Hodgkin 1959, Sutherland 1970), and the sand-dwelling bivalves Amphidesma ventricosum (Rapson 1952) and Scrobicularia plana (Hughes 1970). Phillips (1969) has demonstrated that mortality in the gastropod Dicathais aegrota, which increases in size upshore, is much greater near its upper limit on intertidal limestone platforms than below low water, even though the predation rate at subtidal levels is much greater than on the platforms. Green and Hobson (1970) found that juvenile mortality in the sand- dwelling bivalve Gemma gemma at high shore levels

is greater than that at low levels, while mortality of 1-year-old and older individuals showed the reverse. This disadvantage of juveniles toward high shore levels is reflected in the older age structure of the population in an upshore direction (Green and Hob- son 1970). In the West Indian mud-dwelling bivalve Codakia orbicularis, Jackson (in press) found that large individuals were restricted to the inshore part of its range, and that overall predation rate was much higher in offshore parts of the range than in the physically more rigorous inshore parts.

Among mid to high intertidal barnacles (Connell 1961a, b, 1970) and low to high intertidal mussels (Kitching, Sloan, and Ebling 1959, Seed 1968, Paine 1969), the refuge zone of minimum mortality lies near the upper limit of distribution on the shore and is occupied mostly by old and often large individuals. Predation by gastropods, crabs, starfishes, and other intertidal animals appears to be the most important source of mortality in these sedentary forms (see also Paine 1966), although mass mortality at high levels during hot spells is known in barnacles (Connell 1961a, 1970, Foster 1971). The low to mid intertidal snail Tegula funebralis main- tains a refuge zone of postlarval prereproductives above the upper limit of distribution of the primary predator, the starfish Pisaster ochraceus, while larger individuals migrate down into the zone of overlap with Pisaster (Paine 1969, 1971). Although no ac- curate information about mortality is available for Tegula in the refuge zone, Paine (1971) believes it to be lower than that in the zone of overlap with Pisaster (10% vs. 27.6%).

The above evidence suggests that mortality at high shore levels is principally due to rigors of temperature, desiccation, salinity, and other physical conditions, while predation and other biotic interactions account for much of the mortality at low levels of the shore (see also Connell 1961b, 1970). A possible exception may occur in the predation of the high intertidal limpet Acmaea digitalis by birds, which Giesel (1970) believes to increase in intensity toward higher shore levels.

Because of the decrease in the surface area:volume ratio associated with increasing size, we may reason- ably suppose small individuals to be more susceptible to death from extreme physical conditions, partic- ularly such area-dependent effects as desiccation, than large ones of the same species. Lewis (1954) and Davies (1969) have confirmed this for the limpet Patella vulgata, the latter author further pointing out that allometry during growth accentuates this differ- ence in susceptibility. Davies (1970) has found that large individuals of P. vulgata are more effective in maintaining body temperature below that of the sur- rounding rock when exposed to the air than small ones. In barnacles, Foster (1971) has demonstrated


that ability to withstand desiccation increases with increasing size, but that temperature tolerance does not. In the sand-dwelling gastropod Olivella biplicata, Edwards (1969) has correlated the increase in size toward high shore levels with the demonstrated ability of larger animals to withstand greater desiccation. Boyle (1970) has demonstrated a similar correla- tion between an upshore size increase and greater desiccation tolerance of larger animals in the low to high intertidal chiton Sypharochiton pellisserpentis. The relation between size and the ability to withstand area-dependent physical extremes would, in animals where physical factors are the main source of postlarval prereproductive mortality, accentuate the size gradient resulting from increasing physical rigor in an upshore direction. It is thus plausible that the high incidence of intraspecific upshore size increase among gastropods of the littoral fringe and in high intertidal limpets is because physical rigor is the principal source of postlarval prereproductive mortality among these species.

Little is known of the size component in biotic interactions such as predation and competition. Con- nell (1961a, 1970) demonstrated that the snails Thais lapillus and T. emarginata prefer large barnacles over small ones as prey items; this also appears to be the case with a species of Ocenebra at Asamushi, Japan (Luckens 1970). Connell (1970) also points out that the ability of small prey individuals to hide in places inaccessible to most predators may well in itself cause larger individuals to become more vulnerable to predation. On the other hand, Ebling et al. (1964) have found that a number of species of crabs are not able to prey on Thais and mussels (Mytilus edulis) above a certain size, the latter depending in part on shell thickness and predator size. Similarly, Jackson (in press) found small infaunal bivalves in Jamaican Thalassia beds to be more vulnerable to predation by drilling gastropods than larger bivalves of the same or different species.

If predation is the most important source of mortality for a lower intertidal species, and if predation is most intense at low levels, then the zone of minimal mortality and therefore the greatest concentration of postlarval prereproductives will lie near the upper limit of the vertical range of the prey. This situation would be accentuated if the predator or predators preferred small over large prey. If, on the other hand, the predator preferred large over small prey, postlarval prereproductives would be relatively safe throughout the vertical range, and a shore-level size gradient might not arise.

Although I have tried to argue that postlarval prereproductives should occur in the zone of minimal mortality in the vertical range of a species, nothing has yet been said about the vertical distribution of the larger, sexually mature adults. Paine (1969, 1971)

has shown that the number of calories available for reproduction is greater in adult Tegula funebralis living in the zone of overlap with Pisaster than in comparably sized postlarval prereproductives living in the refuge zone. This may possibly indicate that food or some other resource becomes limiting at high shore levels to animals above a certain size. It may then be selectively advantageous to migrate into a zone where this resource is not limiting, so that more energy may be allocated to reproduction. Predators such as Pisaster, which keep other species from mo- nopolizing the space, create space for the establish- ment and maintenance of algae and other food for the adult snail (Paine 1969) and are thus instrumen- tal in providing an area where resources are not limiting. In cases where the predator prefers large over small prey, resource limitations may restrict adults to low shore levels even though postlarval prereproductives can be found throughout the vertical range of the prey. This type of size gradient is known in at least two low intertidal species of limpet (Shotwell 1950), but whether it is related to the above spec- ulation is still an open question.

Gradients in the intensity of mortality can result in shore-level size gradients in either of two ways: (1) differential mortality of one size group relative to another over the whole or part of the vertical range of a species, or (2) active migration of one size group relative to another. Active size segregation (strategy 2) is possible only in the case of mobile animals such as most rocky-shore gastropods. Differ- ential migration of large individuals in an upshore direction has been observed in Littorina punctata (Evans 1961), L. littorea (Smith and Newell 1955), Acmaea digitalis (Frank 1965), and Patella vulgata on vertical surfaces (Lewis 1954). Blackmore (1969) and Sutherland (1970), working with populations of P. vulgata and A. scabra, respectively, could not detect migration on horizontal surfaces, but did observe an upshore size increase that was related to age. Paine (1969) observed a downward migration of T. funebralis from the top of its vertical range at the onset of sexual maturity.

Sedentary animals such as bivalves and barnacles cannot employ active size segregation to achieve an optimal distribution of size classes and are exposed to passive size selection. In these animals, the seg- ment of the population in the refuge zone or in places inaccessible to the source of mortality often consists of old individuals whose combined repro- ductive rate *must be great enough to replace dead individuals in the areas of minimal mortality and to colonize new parts of the shore.

Matthiessen (1960) has quite convincingly argued that the accumulation of large individuals of the bivalve Mya arenaria in the immediate vicinity of a change in slope of a beach near Quincy, Massachu-


setts, and of small individuals seaward and shoreward of this line, is directly related to size sorting by waves during storms when animals are dislodged from the sediment in which they are normally buried. Such particle sorting may well take place in many other bivalves inhabiting soft substrata, and can thus po- tentially modify the effects of size-dependent mortality and of environmental gradients.

The present interpretation of intraspecific shore- level size gradients is based principally on shore-level gradients in mortality of postlarval prereproductives and on the assumption that the latter will inhabit that part of the vertical range of the species where mortality is lowest. This assumption remains to be tested, and our knowledge of the physical and biotic gradients on the shore is far from adequate. In addition, it is by no mean certain that other important considerations have not been overlooked. Sacchi (1969b) attributes shore-level size gradients and accompanying vertical migration to advantages associated with the resulting decreased population density. In discussing the size increase toward high shore levels in the sand- beach gastropod Olivella biplicata, Edwards (1969) argues that the probability of two adult individuals encountering one another and copulating is greater in the presence of size-class segregation than in its absence, and points out that the principal prey item of the species, the polychaete Thoracophelia mucronata, is similarly size selected according to shore level (Dales 1952). Size gradients of a similar nature are, however, also to be found among gastropods which do not practice internal fertilization, such as archaeogastropod limpets, and among microphagous forms whose food is almost certainly not size selected according to shore level.

It may well be naive to seek a universal explana- tion valid for all intraspecific shore-level size gradients in intertidal animals. Imperfect as the inter- pretations set forth in this paper may be, however, they may suggest approaches not hitherto considered in the study of these gradients. A greater understanding of such size gradients and associated phenomena may lead to a better understanding of how primary physical gradients in the environment influence community structure.

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